Glomerular hemodynamics before and after release of 24- hour bilateral ureteral obstruction
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1 Kidney International, Vol. 17 (1980), pp Glomerular hemodynamics before and after release of 24- hour bilateral ureteral obstruction ANTONIO DAL CANTON, ARIBERTO CORRADI, RODOLFO STANZIALE, GIANFRANCO MARUCCIO, and LuIGI MIGONE Institute of Medical Clinic and Nephrology, University of Parma, Italy Glomerular hemodynamics before and after release of 24-hour bilateral ureteral obstruction. Glomerular hemodynamics were studied, by micropuncture, in Munich-Wistar rats submitted to 24-hour bilateral ureteral ligation (BUL). Glomerular capillary pressure (PG), intratubular pressure (PT), and pressure in the first order peritubular capillaries (EAP) were measured with a servonulling device. Single nephron filtration fraction (SNFF) was calculated from arterial and peritubular blood protein concentrations. Single nephron glomerular filtration rate (SNGFR) was both measured by conventional micropuncture techniques and calculated from efferent arteriole blood flow and SNFF. Afferent arteriole blood flow (AABF) and resistance of afferent (Ra) and efferent (Re) arteriole were calculated. Measurements were repeated in the left kidney after releasing the ureter. Sham operated rats were used as control. BUL caused a fall in SNGFR (from to 40.7 [sam] 6.0 nllmin/kg body wt), accounted for by a rise in PT (from to mm Hg), glomerular hemodynamics (particularly PG and AABF) being unchanged. A marked increase in Ra (from to dynes sec cm 5) occurred after releasing the ureter, lessening both PG and AABF. Therefore, a low SNGFR was maintained despite the concomitant normalization of PT. Héinodynamique glomérulaire avant et après Ia levee d'une obstruction urétérale bilatérale de 24 heures. L'hémodynamique glomérulaire a été étudiée par microponction chez des rats Munich-Wistar soumis a une ligature urétérale bilatérale de 24 heures (BUL). La pression capillaire glomerulaire (PG), La pression intratubulaire (PT) et Ia pression dans les capillaires péritubulaires de premier ordre ont été mesurées au moyen d'un dispositif a zero asservi. La fraction de filtration des néphrons (SNFF) a été calculée a partir des concentrations de protéines dans Ic sang artériel et péritubulaire. Le debit de filtration glomérulaire des néphrons (SNGFR) a été mesuré par les techniques habituelles de microponction et calculé a partir du debit dans l'artériole efférente et de SNFF. Le debit dans l'artériole afférente (AABF) et Ia résistance des arterioles afférente (Ra) et efférente (Re) ont etc calculés. Les mesures ont été faites a nouveau sur le rein gauche après Ia levee de l'obstruction urétérale. Des rats ayant subi un simulacre d'intervention ont servi de contrôles. BUL a déterminc une dimunition de SNGFR (de 101,8 9,7 a 40,7 [5EM] 6,0 nllmin/kg poids humide) dont rend compte une augmentation de PT (de 14,1 0,7 a 28,9 3,1 mmhg), les paramètres de l'hcmodynamique glomérulaire (PG et AABF particulièrement) n'étant pas affectés. Une augmentation importante de Ra (de 6,6 0,7,à ,5 dynes sec cm-5) se produit après Ia levee de l'obstacle urctcral, diminuant a Ia fois PG et AABF. Un SNGFR bas est donc maintenu malgré une normalisation concomitante de PT. Recently, we have shown that unilateral ureteral obstruction for 24 hours produces a marked increase in afferent arteriole resistance, which is not reversed by ureteral release. The ensuing cortical ischemia accounts for a fall in glomerular filtration rate, both in the whole kidney (GFR) and in the single nephron (SNGFR) [1]. So far, the effects of 24-hour bilateral ureteral ligation (BUL) have not been adequately investigated. No measurement of glomerular filtration rate or of renal blood flow has been reported during BUL. After releasing one ureter, a decrease in both GFR and SNGFR has been demonstrated [2-5]. Scanty and controversial data are instead available on glomerular plasma flow, which has been found to be either normal [5], or consistently reduced [2]. The present study was designed to evaluate the glomerular hemodynamics and to measure SNGFR in the rat kidney both before and after release of 24- hour bilateral ureteral obstruction. Methods Sixteen nonfasted Munich- Wistar rats with glomeruli on the kidney surface [6] were anesthetized lightly with ether. The abdomen was opened via a midline laparotomy, and both the ureters were ligated in nine rats about 1 cm above the bladder, and the other seven rats were sham-operated and used for control. The rats were housed in their cages and left without food and water for 24 hours, when they were anesthetized again with sodium Received for publication April 23, 1979 and in revised form August 6, /80/ $ by the International Society of Nephrology 491
2 492 Dat Canton et a! pentobarbital (Nembutal, 60 mg/kg body wt, i.p.) and prepared for micropuncture, as previously described [7]. After the surgical preparation, an i.v. infusion of bicarbonate-saline solution (sodium chloride, 110 meq/liter; sodium bicarbonate, 28 meq/liter; potassium chloride, 5 meq/liter) containing inulin (5%) was begun at an infusion rate of 0.01 mllmin. The infusion rate was increased to 0.02 ml/ mm after releasing the left ureter in six rats in which postobstructive studies were performed. One hour was allowed for equilibration before starting micropuncture measurements. Ureteral obstruction studies. In nine rats with 24- hour BUL, glomerular capillary pressure (PG), intratubular pressure (PT), and pressure in the first order peritubular capillaries (so-called efferent arteriole pressure, EAP) were measured with a servonulling device (Instrumentation for Physiology and Medicine, San Diego, California) and recorded on a dual-channel recorder (Hewlett-Packard, 7702 B) together with blood pressure from a femoral artery (BP). Timed, complete collections of tubular fluid were obtained for measurement of SNGFR [8]. The number of collections (and of SNGFR measurements) was limited because a long time (5 to 10 mm) was required to obtain adequate volumes of tubular fluid. Moreover, the oil block injected into the tubule sometimes did not move downstream so that collection was impossible. Therefore, SNGFR was calculated also from the efferent arteriole plasma flow (EAPF) and single nephron filtration fraction (SNFF) according to the equation EAPF SNGFR = EAPF SNFF This method was previously validated in our laboratory [8] and required timed, complete collections of blood from the welling points of superficial efferent arterioles, for direct measurement of efferent arteriole blood flow (EABF) from which EAPF was calculated. Postobstructive studies. In six rats, when the measurements of the obstructive period were completed, the left ureter was clamped just below the pelvis and cannulated proximally to the ligation with polyethylene (PE-50) tubing (Clay Adams) connected to a pressure transducer. The clamp was then released, and the ureteral pressure (Pt) was recorded. The obstruction was relieved in the left kidney by cutting the PE-50 catheter used for Pu measurement. One hour was allowed before starting the following measurements: (a) GFR and sodium excretion rate (UvaV) of the left kidney. Urine was (1) collected under mineral oil; arterial blood samples were obtained from the femoral artery at the beginning and at the end of clearance periods. (b) Micropuncture measurements. Timed, complete collections of tubular fluid and of peritubular blood were carried out, and micropressures were recorded as during the obstruction. Control studies. Measurements as described above were performed also in the left kidney of seven control rats, 24 hours after sham-operation. Analytical determinations and calculations. Urine volume was obtained by weight. The volumes of fluid and blood collected from proximal tubules and efferent arterioles, respectively, were estimated from the length of the fluid column in a calibrated constant-bore quartz tubing of approximately 100 ID. (Fnedrick and Dimmock, Millville, New Jersey). The concentration of chemical inulin in tubular fluid was measured by the microfluorescent method of Vurek and Pegram; chemical inulin concentrations in plasma and urine were determined by the diphenylamine method. Plasma protein concentration was measured by Lowry's method; a microadaptation of the same method was used to measure protein concentration in blood collected from efferent arterioles. Sodium concentration in urine was measured by flame photometry [6]. SNGFR, single nephron filtration fraction (SNFF), effective filtration pressure at the afferent end of the glomerulus (EFPa), flows and resistances of single afferent and efferent arterioles were calculated as described in our previous papers [1, 8]. Results are presented as the means SEM. Results Ureteral obstruction studies (Table 1). PG was similar in control and in obstructed rats. In the latter, PT was increased from to mm Hg (P < 0.005). The rise in PT was responsible for a reduction in both hydrostatic pressure gradient across glomerular capillaries (PG) and EFPa. During BUL, no difference was found in afferent arteriole resistance (Ra) nor in afferent arteriole blood flow (AABF). SNGFR fell from to ni/mm/kg body wt (P < 0.00 I). The latter value was calculated as the mean of averaged measurements of SNGFR in single rats, with conventional technique and with efferent arteriole blood collection. As shown in Table 2, in fact, similar results were obtained with the two methods. Afferent arteriole plasma flow (AAPF) being unchanged, the decrease in SNGFR accounted for a reduction in SNFF, which was paralleled by a fall in both hema-
3 Glornerular hemodynamics in ureteral obstruction 493 Table 1. Pressures, flows, protein concentrations, hematocrits, and resistances in control conditions and after 24 hours of bilateral ureteral obstructiona Ureteral Control obstruction P Bodywt,g NS BP,rnmHg NS P,,n,,nHg (N = 26) (N 31) NS PT,rnmHg (N = 39) (N = 48) <0.005 EAP,rnmHg (N = 29) (N = 37) NS PG,mmHg <0.001 EFPa,ininHg <0.001 SNGFR, n//mm/kg body WI (N = 42) (N = 68) <0.001 AABF,nI/mmn/kgbodywt NS AAPF, ni/mm/kg body wi NS EABF,nI/min/kgbodvwt NS EAPF,nllmmn/kgbodywt NS P,g/dl NS Pe,g/dl (N = 33) (N = 45) <0.001 ira,mmhg NS lte,mmhg < Te/LP NS HCta, % NS Hcte, % <0.005 SNFF <0.001 Ra,dynes sec cm NS Re,dynes sec cm NS a Abbreviations used are: BP, arterial blood pressure; P0, glomerular capillary pressure (hydrostatic); P1, intratubular pressure; EAP, pressure in the first order peritubular capillary (so-called efferent arteriole pressure); P0, hydrostatic pressure gradient across glornerular capillaries; EFPa, effective filtration pressure at the afferent end of the glomerulus; SNGFR, single nephron filtration rate; AABF, afferent arteriole blood flow; AAPF, afferent arteriole plasma flow; EABF, efferent arteriole blood flow; EAPF, efferent arteriole plasma flow; Pa, systemic arterial protein concentration; Pa, oncotic pressure in afferent and efferent arteriole; HCta and HCte, hematocrit in afferent and efferent arteriole; SNFF, single nephron filtration fraction; Ra and Re, resistance of single afferent and efferent arteriole. All values are means SEM. The results are given as the mean values of the averaged measurements in single rats. NS denotes not significant (P> 0.05) with unpaired Student's t test. Numbers in parentheses are numbers of observations. tocrit (HCte) and protein concentration (Pe) at the exit of the efferent arteriole. Consequently, also peritubular capillary oncotic pressure (Te)was lowered. Ureteral obstruction caused no change in efferent arteriole resistance (Re) or in EABF. At the efferent end of the glomerulus, glomerular pressure Table 2. Average SNGFR in single rats, measured with conventional micropuncture technique and from Equation P Rat no Mean SEM SNGFR, ni/mm/kg body wt Conventional technique Equation 1 Average 22.8 (N = 3) 60.1 (N = 4) 30.4 (N = 3) 51.2 (N = 4) 23.9 (N = 2) 36.7 (N = 4) 22.1 (N = 4) 43.1 (N = 3) 64.5 (N = 5) (N = 3) 47.5 (N = 3) 18.6 (N = 5) 66.8 (N = 4) 29.3 (N = 5) 46.3 (N 4) 17.9 (N = 4) 46.9 (N = 4) 78.5 (N = 4) equilibrium was taking place in control conditions as well as during BUL, the ratio i'lpg not being different from 1 (P > 0.1). Finally, BUL caused a rise in P, from to mm Hg (P < 0.005). Posrobstructive studies (Tables 3 and 4). The relief of the ureter caused a fall in PT, from to mm Hg (P < ). PG decreased, but to a lesser degree than PT, so that both ZPG and EFPa were increased. A marked rise in Ra (from to dyne sec cm5) determined a fall in both AABF and AAPF. SNGFR was maintained low, measuring nl/minlkg body wt during BUL, vs nllminlkgbodywt in the postobstructive conditions (P > 0.05). The increase in SNFF was accompanied by a rise in both Hcte and Pe. Re was slightly augmented, but the difference did not attain statistical significance (P > 0.05). Although GFR was markedly reduced in the released kidney of bilaterally obstructed rats, in the latter both urinary volume and urinary sodium excretion rate were higher than they were in the con- a Numbers in parentheses are numbers of observations. trol kidney of sham-operated rats (Table 4).
4 494 Dal Canton et at Table 3. Pressures, flows, resistances, protein concentrations, and hematocrits during 24-hour bilateral obstruction and the postobstructive perioda Obstructive period Postobstructive period BP,mmHg NS PG,mmHg <0.01 (N=19) (N=17) PT, mm Hg <0.005 (N=29) (N=29) EAP,mmHg <0.005 (N=21) (N=18) AP,mmHg <0.01 EFPa,mmHg <0.01 SNGFR,nl/minlkgbodywt NS (N=26) (N=22) AABF,nllmin/kgbodywt <0.005 AAPF,nllmin/kgbodywt <0.005 EABF,nllmin/kgbodywt <0.005 EAPF,nl/min/kgbodywt <0.005 Pa,g/dl NS Pe,g/dl <0.025 (N = 21) (N = 18) <0.005 i,mmhg NS 1Te,mm Hg < Te/PG NS Hcta,% NS Hcte, % <0.025 SNFF <0.025 Ra,dynes sec cm <0.005 Re,dynes sec cm NS Abbreviations are defined in Table 1. All values are means SEM. The results are given as the mean values of the averaged measurements in single rats. NS denotes not significant with paired Student's t test. Numbers in parentheses are numbers of observations. P Discussion In the present study, 24 hours after bilateral ureteral ligation, a fall in SNGFR was observed, accounted for by a decrease in effective filtration pressure. The latter was entirely due to a rise in PT, gbmerular hemodynamics, and particularly PG being unmodified. The reduction in SNGFR persisted in the postobstructive period, but the reason was quite different. In fact, after releasing the ureter, we noted a striking increase in afferent arteriole resistance, Table 4. Urine flow, sodium excretion and inulin clearance from the left kidney of control (C) and previously obstructed (P0) rats Inulin clearance mi/mm V pi/min UNaV peq/min C P P <0.01 <0.05 <0.05 a Values are means SEM. Abbreviations used are: V, urine flow; UNaV, urinary sodium excretion. which decreased both PG and glomerular plasma flow. The decrease in P0 was responsible for a lower than normal effective filtration pressure, which undoubtedly contributed to impair SNGFR. EFPa, however, was raised with respect to the previous, that is, obstructive setting, because the reduction of PG was overwhelmed by a fall in PT. Therefore, the maintenance of a low SNGFR was mainly accounted for by the decrease in glomerular plasma flow, in accordance to the high plasma-flow dependence of SNGFR in the Munich-Wistar rat [9], especially when filtration pressure equilibrium is taking place [10]. Because the latter obtained both in control and in obstructed rats, before and after releasing the ureter, a definite value of the ultrafiltration coefficient (Kr) could not be calculated [11]. Thus, we cannot exclude that some decrease in Kf contributed to reduce SNGFR. The normality of glomerular hemodynamics during BUL stands in interesting contrast to the changes observed during unilateral ureteral ligation (UUL) in our laboratory [1]. As shown in Table 5, in fact, after 24 hours of UUL, a marked increase in afferent arteriole resistance takes place, accounting
5 Glomerular hemodynamics in ureteral obstruction 495 Table 5. Comparison of the effects of unilateral (UUL) and bilateral (BUL) ureteral ligation on glomerular hemodynamicsa PT P6 AAPF R, SNGFR I I 24-hr UUL 24-hrBUL I I = = = a Abbreviations are defined in Table 1. Symbols are 1, increased; =, unchanged; I,decreased. Number of arrows reflect the entity of the change. for a fall both in glomerular capillary hydrostatic pressure and in glomerular plasma flow. Therefore, the cause of the reduction in GFR is quite different in BUL and UUL, being a rise in PT in the former and a rise in Ra in the latter. The reason for this difference is not apparent from our studies. It has been suggested that the increase in Ra during UUL is accounted for by a reduced prostaglandin delivery to the superficial arterioles, secondary to a fall in distal tubular flow rate [I]. Prostaglandins, in fact, enter Henle's loops from the medullary interstitium, moving to the cortex via the distal tubular fluid [12]. Tubular flow rate was not measured in our experiments, nor was it reported by others, during BUL. After releasing the ureter, however, a marked decrease in proximal fractional reabsorption was found, maintaining distal tubular flow despite a fall in SNGFR [3, 5]. Although the preobstructive and postobstructive conditions cannot be soundly compared, because the relief of the obstruction modifies the hydrodynamic pressure gradient along the urinary spaces (that is, the driving force for tubular flow), it is possible that the cortical migration of prostaglandins was not as reduced during BUL as it was during UUL. Alternatively, at least two other vasodilating mechanisms may be operating in BUL, but not in UUL. The first possibility is that an extracellular volume expansion may occur in 24 hours of anuria. To prevent this possibility, however, we held our rats with BUL without water and food during the obstruction and we infused them at a low infusion rate (0.01 ml/min) to replace surgical fluid losses during micropuncture. Furthermore, no difference in blood protein concentration nor in hematocrit was found between control and obstructed rats, which would reasonably exclude in the latter an extracellular volume expansion. The second possibility is that some unidentified vasodilating substance, which is normally excreted in urine, is retained during BUL. The existence of such a substance was shown by the experiments of Harris and Yarger [13] and is suggested also by the diuretic and vasodilating effects of urine intravenously reinfused in the rat [14]. In the present study, a polyuria was taking place after releasing the ureter. Previous studies have shown that such a postobstructive diuresis is due to a fall in sodium reabsorption both in the proximal tubule and in the loop of Henle, raising distal sodium delivery [5]. According to the tubuloglomerular feedback hypothesis [15], this sudden increase in sodium chloride delivery to the distal tubule can well account for the marked increase in afferent arteriole resistance observed soon after releasing the ureter, as first suggested by Wright [16]. Alternatively, the ureter-obstructed kidney may be producing a vasoconstrictor material, as shown in isolated perfused rabbit kidneys by Morrison, Nishikawa, and Needleman [17]. Such a constrictor identified as thromboxane A2 may be antagonized in the anuric condition, as previously discussed, and manifest its effects only after ureteral release. Finally, we emphasize that the afferent vasoconstriction was not accompanied by any change in efferent arteriole resistance, This appears in agreeinent with our previous studies showing that superficial efferent arterioles behave as passive vessels; that is, they are unable both to dilate and to constrict in response to neural and/or humoral stimuli [7]. Reprint requests to Dr. A. Dal Canton, Division of Nephrology, Nuovo Policlinico, via Parsini, 80131, Naples, Italy References 1. DAL CANTON A, CORRADI A, STANZIALE R, MARuccIo GF, MIGONE L: Effects of 24-hour unilateral ureteral obstruction on glomerular hemodynamics in rat kidney. Kidney mt 1979, in press 2. YARGER WE, AYNEDJAN MS, BANK N: A micropuncture study of post-obstructive diuresis in the rat. J Cliii invest 51: , BLJERKERT J, ALEXANDER E, PURKERSON ML, KLAHAR 5: On the site of decreased fluid reabsorption after release of ureteral obstruction in the rat. J Lab Cliii Med 87: , JAENIKE JR: The renal functional defect of postobstructive nephropathy. J Clin Invest 51: , MCDOUGAL WS, WRIGHT FS: Defect in proximal and distal sodium transport in post-obstructive diuresis. Kidney mt 2: , ANDREUCCI VE: Manual of Renal Micropuncture. Naples, Idelson Publishers, ANDREUCCI ye, DAL CANTON A, CORRADI A, STANZIALE R, MIGONE L: Role of efl'erent arterioles in glomerular hemodynamics of superficial nephrons. Kidney mt 9: , DAL CANTON A, STANZIALE R, CORRADI A, ANDREUCCI ye, MIGONE L: Effects of acute ureteral obstruction on glomerular hemodynamics in rat kidney. Kidney mt 12: , 1977
6 496 Dal Canton et a! 9. BRENNER BM, TROY JL, DAUGHARTY TM, DEEN WM, ROB- ERTSON CR: Dynamics of glomerular ultrafiltration in the rat: II. Plasma flow dependence of GFR. Am J Physiol 223: , TUCKER BJ, BLANTZ RC: An analysis of the determinants of nephron filtration rate. Am J Physiol 232:F477-F483, DEEN WM, ROBERTSON CR, BRENNER BM: A model of gbmerular ultrafiltration in the rat. Am J Physiol 223: , WILLIAMS WM, FR0LIcH JC, NIEs AS, OATES JA: Urinary prostaglandins: Site of entry into renal tubular fluid. Kidney mt 11: , HARRIS RH, YARGER WE: The pathogenesis of post-obstructive diuresis: The role of circulating natriuretic factors, including urea. J Clin Invest 56: , HARRIS RH, YARGER WE: Urine-reinfusion natriuresis: evidence for potent natriuretic factors in rat urine. Kidney mt 11:93 105, SCHNERMANN J, PERSSON AEG, AGERUP B: Tubuloglomerular feedback. Nonlinear relation between glomerular hydrostatic pressure and loop of Henle perfusion rate. J Gun Invest 52: , WRIGHT FS: Intrarenal regulation of glomerular filtration rate. N EnglJ Med 291: , MORRIsON AR, NISHIKAWA K, NEEDLEMAN P: Unmasking of Thromboxane A2 synthesis by ureteral obstruction in the rabbit kidney. Nature 267: , 1977
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